Abstract
Interest in social learning has been fueled by claims of culture in wild animals. These remain controversial because alternative explanations to social learning, such as asocial learning or ecological differences, remain difficult to refute. Compared with laboratory-based research, the study of social learning in natural contexts is in its infancy. Here, for the first time, we apply two new statistical methods, option-bias analysis and network-based diffusion analysis, to data from the wild, complemented by standard inferential statistics. Contrary to common thought regarding the cognitive abilities of prosimian primates, our evidence is consistent with social learning within subgroups in the ring-tailed lemur (Lemur catta), supporting the theory of directed social learning (Coussi-Korbel & Fragaszy, 1995). We also caution that, as the toolbox for capturing social learning in natural contexts grows, care is required in ensuring that the methods employed are appropriate-in particular, regarding social dynamics among study subjects. Supplemental materials for this article may be downloaded from http://lb.psychonomic-journals.org/content/supplemental.
Article PDF
Similar content being viewed by others
References
Akaike, H. (1973). Information theory and an extension of the maximum likelihood principle. In B. N. Petrov & F. Csáki (Eds.), Proceedings of the Second International Symposium on Information Theory (pp. 267–281). Budapest: Akadémiai Kiadó.
Altman, D. G. (1991). Practical statistics for medical research. London: Chapman & Hall/CRC.
Anderson, J. R., Fornasieri, I., Ludes, E., & Roeder, J.-J. (1992). Social processes and innovative behaviour in changing groups of Lemur fulvus. Behavioural Processes, 27, 101–112. doi:10.1016/0376-6357(92)90020-E
Bonnie, K. E., & de Waal, F. B. M. (2006). Affiliation promotes the transmission of a social custom: Handclasp grooming among captive chimpanzees. Primates, 47, 27–34. doi:10.1007/s10329-005-0141-0
Boogert, N. J., Reader, S. M., Hoppitt, W., & Laland, K. N. (2008). The origin and spread of innovations in starlings. Animal Behaviour, 75, 1509–1518. doi:10.1016/j.anbehav.2007.09.033
Boogert, N. J., Reader, S. M., & Laland, K. N. (2006). The relation between social rank, neophobia and individual learning in starlings. Animal Behaviour, 72, 1229–1239. doi:10.1016/j.anbehav.2006.02.021
Boyd, R., & Richerson, P. J. (1985). Culture and the evolutionary process. Chicago: University of Chicago Press.
Budnitz, N., & Dainis, K. (1975). Lemur catta: Ecology and behavior. In I. Tattersall & R. W. Sussman (Eds.), Lemur biology (pp. 219–235). New York: Plenum Press.
Byrne, R. W. (1994). The evolution of intelligence. In P. J. B. Slater & T. R. Halliday (Eds.), Behaviour and evolution (pp. 223–265). New York: Cambridge University Press.
Coussi-Korbel, S., & Fragaszy, D. M. (1995). On the relation between social dynamics and social learning. Animal Behaviour, 50, 1441–1453. doi:10.1016/0003-3472(95)80001-8
Day, R. L. (2003). Innovation and social learning in monkeys and fish: Empirical findings and their application to reintroduction techniques. Unpublished doctoral dissertation, University of Cambridge, Cambridge, U.K.
Dean, L., Kendal, R. L., Hoppitt, W., & Laland, K. N. (2010). Sex ratio affects sex-specific innovation and learning in captive ruffed lemurs (Varecia variegata spp.). Manuscript submitted for publication.
Flynn, E., & Whiten, A. (2010). Studying children’s social learning experimentally “in the wild.” Learning & Behavior, 38, 284–296.
Fornasieri, I., Anderson, J. R., & Roeder, J.-J. (1990). Responses to a novel food acquisition task in three species of lemurs. Behavioural Processes, 21, 143–156. doi:10.1016/0376-6357(90)90021-7
Franz, M., & Nunn, C. L. (2009). Network-based diffusion analysis: A new method for detecting social learning. Proceedings of the Royal Society B, 276, 1829–1836. doi:10.1098/rspb.2008.1824
Franz, M., & Nunn, C. L. (2010). Investigating the impact of observation errors on the statistical performance of network-based diffusion analysis. Learning & Behavior, 38, 235–242.
Gould, L. (1997). Affiliative relationships between adult males and immature group members in naturally occurring ringtailed lemurs (Lemur catta). American Journal of Physical Anthropology, 103, 163–171. doi:10.1002/(SICI)1096-8644(199706)103:2<163::AID-AJPA3τ;3.0.CO;2-V
Holzhaider, J. C., Hunt, G. R., & Gray, R. D. (2010). Social learning in New Caledonian crows. Learning & Behavior, 38, 206–219.
Hopper, L. M., Spiteri, A., Lambeth, S. P., Schapiro, S. J., Horner, V., & Whiten, A. (2007). Experimental studies of traditions and underlying transmission processes in chimpanzees. Animal Behaviour, 73, 1021–1032. doi:10.1016/j.anbehav.2006.07.016
Hoppitt, W., Boogert, N. J., & Laland, K. N. (2010). Detecting social transmission in networks. Journal of Theoretical Biology, 263, 544–555. doi:10.1016/j.jtbi.2010.01.004
Hoppitt, W., Kandler, A., Kendal, J. R., & Laland, K. N. (2010). The effect of task structure on diffusion dynamics: Implications for diffusion-curve and network-based analyses. Learning & Behavior, 38, 243–251.
Hoppitt, W., & Laland, K. N. (2008). Social processes influencing learning in animals: A review of the evidence. Advances in the Study of Behavior, 38, 105–165. doi:10.1016/S0065-3454(08)00003-X
Horner, V., & Whiten, A. (2005). Causal knowledge and imitation/emulation switching in chimpanzees (Pan troglodytes) and children (Homo sapiens). Animal Cognition, 8, 164–181. doi:10.1007/s10071-004-0239-6
Hosey, G. R., Jacques, M., & Pitts, A. (1997). Drinking from tails: Social learning of a novel behaviour in a group of ring-tailed lemurs (Lemur catta). Primates, 38, 415–422. doi:10.1007/BF02381881
Jolly, A. (1966). Lemur behavior: A Madagascar field study. Chicago: University of Chicago Press.
Jolly, A., & Pride, E. (1999). Troop histories and range inertia of Lemur catta at Berenty, Madagascar: A 33-year perspective. International Journal of Primatology, 20, 359–373. doi:10.1023/A:1020548620372
Kappeler, P. M. (1987). The acquisition process of a novel behavior pattern in a group of ring-tailed lemurs (Lemur catta). Primates, 28, 225–228. doi:10.1007/BF02382571
Kasper, C., & Voelkl, B. (2009). A social network analysis of primate groups. Primates, 50, 343–356. doi:10.1007/s10329-009-0153-2
Kendal, J. R., Kendal, R. L., & Laland, K. N. (2007). Quantifying and modelling social learning processes in monkey populations. International Journal of Psychology & Psychological Therapy, 7, 123–138.
Kendal, R. L., Coolen, I., & Laland, K. N. (2009). Adaptive tradeoffs in the use of social and personal information. In R. Dukas & J. M. Ratcliffe (Eds.), Cognitive ecology II (pp. 249–271). Chicago: University of Chicago Press.
Kendal, R. L., Coolen, I., van Bergen, Y., & Laland, K. N. (2005). Trade-offs in the adaptive use of social and asocial learning. Advances in the Study of Behavior, 35, 333–379. doi:10.1016/S0065-3454(05)35008-X
Kendal, R. L., Kendal, J. R., Hoppitt, W., & Laland, K. N. (2009). Identifying social learning in animal populations: A new “option-bias” method. PLoS ONE, 4, e6541. doi:10.1371/journal.pone.0006541
Koyama, N., Ichino, S., Nakamichi, M., & Takahata, Y. (2005). Long-term changes in dominance ranks among ring-tailed lemurs at Berenty Reserve, Madagascar. Primates, 46, 225–234. doi:10.1007/s10329-005-0155-7
Krützen, M., Mann, J., Heithaus, M. R., Connor, R. C., Bejder, L., & Sherwin, W. B. (2005). Cultural transmission of tool use in bottlenose dolphins. Proceedings of the National Academy of Sciences, 102, 8939–8943. doi:10.1073/pnas.0500232102
Laland, K. N. (2004). Social learning strategies. Learning & Behavior, 32, 4–14.
Laland, K. N., Kendal, J. R., & Kendal, R. L. (2009). Animal culture: Problems and solutions. In K. N. Laland & B. G. Galef (Eds.), The question of animal culture (pp. 174–197). Cambridge, MA: Harvard University Press.
Leca, J.-B., Gunst, N., & Huffman, M. A. (2007). Japanese macaque cultures: Inter- and intra-troop behavioural variability of stone handling patterns across 10 troops. Behaviour, 144, 251–281. doi:10.1163/156853907780425712
Lefebvre, L., & Palameta, B. (1988). Mechanisms, ecology, and population diffusion of socially learned, food-finding behavior in feral pigeons. In T. R. Zentall & B. G. Galef, Jr. (Eds.), Social learning: Psychological and biological perspectives (pp. 141–164). Hillsdale, NJ: Erlbaum.
Matthews, L. J. (2009). Intragroup behavioral variation in white-fronted capuchin monkeys (Cebus albifrons): Mixed evidence for social learning inferred from new and established analytical methods. Behaviour, 146, 295–324. doi:10.1163/156853909X410937
McGrew, W. C. (1998). Culture in nonhuman primates? Annual Review of Anthropology, 27, 301–328. doi:10.1146/annurev.anthro.27.1.301
Moreno, J. L. (Ed.) (1960). The sociometry reader. Glencoe, IL: Free Press.
Nahallage, C. A. D., & Huffman, M. A. (2007). Age-specific functions of stone handling, a solitary-object play behavior, in Japanese macaques (Macaca fuscata). American Journal of Primatology, 69, 267–281. doi:10.1002/ajp.20348
Nakamichi, M., Rakototiana, M. L. O., & Koyama, N. (1997). Effects of spatial proximity and alliances on dominance relations among female ring-tailed lemurs (Lemur catta) at Berenty Reserve, Madagascar. Primates, 38, 331–340. doi:10.1007/BF02381620
Newman, M. E. J., & Girvan, M. (2004). Finding and evaluating community structure in networks. Physical Review, E69, 026113. doi:10.1103/PhysRevE.69.026113
Overdorff, D. J., Erhart, E. M., & Mutschler, T. (2005). Does female dominance facilitate feeding priority in black-and-white ruffed lemurs (Varecia variegata) in southeastern Madagascar? American Journal of Primatology, 66, 7–22. doi:10.1002/ajp.20125
Perry, S. (2009). Conformism in the food processing techniques of white-faced capuchin monkeys (Cebus capucinus). Animal Cognition, 12, 705–716. doi:10.1007/s10071-009-0230-3
Perry, S., Baker, M., Fedigan, L., Gros-Louis, J., Jack, K., MacKinnon, K. C., et al. (2003). Social conventions in wild white-faced capuchin monkeys: Evidence for traditions in a neotropical primate. Current Anthropology, 44, 241–268. doi:10.1086/345825
Reader, S. M. (2004). Distinguishing social and asocial learning using diffusion dynamics. Learning & Behavior, 32, 90–104.
Reader, S. M., & Biro, D. (2010). Experimental identification of social learning in wild animals. Learning & Behavior, 38, 265–283.
Rendell, L., & Whitehead, H. (2001). Culture in whales and dolphins. Behavioral & Brain Sciences, 24, 309–382. doi:10.1017/S0140525X0100396X
Santos, L. R., Mahajan, N., & Barnes, J. L. (2005). How prosimian primates represent tools: Experiments with two lemur species (Eulemur fulvus and Lemur catta). Journal of Comparative Psychology, 119, 394–403. doi:10.1037/0735-7036.119.4.394
Sapolsky, R. M. (2005). The influence of social hierarchy on primate health. Science, 308, 648–652. doi:10.1126/science.1106477
Sargeant, B. L., & Mann, J. (2009). From social learning to culture: Intrapopulation variation in bottlenose dolphins. In K. N. Laland & B. G. Galef (Eds.), The question of animal culture (pp. 152–173). Cambridge, MA: Harvard University Press.
Swaney, W., Kendal, J., Capon, H., Brown, C., & Laland, K. N. (2001). Familiarity facilitates social learning of foraging behaviour in the guppy. Animal Behaviour, 62, 591–598. doi:10.1006/anbe.2001.1788
Thornton, A., & Malapert, A. (2009). Experimental evidence for social transmission of food acquisition techniques in wild meerkats. Animal Behaviour, 78, 255–264. doi:10.1016/j.anbehav.2009.04.021
van Schaik, C. P., Ancrenaz, M., Borgen, G., Galdikas, B., Knott, C. D., Singleton, I., et al. (2003). Orangutan cultures and the evolution of material culture. Science, 299, 102–105. doi:10.1126/science.1078004
Warner, R. R. (1988). Traditionality of mating-site preferences in a coral reef fish. Nature, 335, 719–721. doi:10.1038/335719a0
White, F. J., Overdorff, D. J., Keith-Lucas, T., Rasmussen, M. A., Kallam, W. E., & Forward, Z. (2007). Female dominance and feeding priority in a prosimian primate: Experimental manipulation of feeding competition. American Journal of Primatology, 69, 295–304. doi:10.1002/ajp.20346
Whitehead, H. (2009). How might we study culture? A perspective from the ocean. In K. N. Laland & B. G. Galef (Eds.), The question of animal culture (pp. 125–151). Cambridge, MA: Harvard University Press.
Whiten, A. (2009). The identification and differentiation of culture in chimpanzees and other animals: From natural history to diffusion experiments. In K. N. Laland & B. G. Galef (Eds.), The question of animal culture (pp. 99–124). Cambridge, MA: Harvard University Press.
Whiten, A., Goodall, J., McGrew, W. C., Nishida, T., Reynolds, V., Sugiyama, Y., et al. (1999). Cultures in chimpanzees. Nature, 399, 682–685. doi:10.1038/21415
Whiten, A., Horner, V., & de Waal, F. B. M. (2005). Conformity to cultural norms of tool use in chimpanzees. Nature, 437, 737–740. doi:10.1038/nature04047
Whiten, A., Spiteri, A., Horner, V., Bonnie, K. E., Lambeth, S. P., Schapiro, S. J., & de Waal, F. B. M. (2007). Transmission of multiple traditions within and between chimpanzee groups. Current Biology, 17, 1038–1043. doi:10.1016/j.cub.2007.05.031
Author information
Authors and Affiliations
Corresponding author
Additional information
We gratefully acknowledge Jennifer Mayer, M. Jean DeHeaulme, Alison Jolly, Nirina Rasiminalala, and all of the staff at Berenty Reserve for assistance with the lemur field study; Natalie Kelly and Jennifer Mayer for assisting in interobserver reliability; Rebecca Antworth and Elizabeth King for task design; and Steven Yesson, who made task copies. Sincere thanks also to Will Hoppitt for ongoing advice regarding extending the option-bias analysis method and to Carel van Schaik for useful comments and suggestions. The work presented here was supported by a British Academy Small Research Grant to D.M.C.; a Royal Society Dorothy Hodgkin Fellowship to R.L.K.; an RCUK Research Fellowship to J.R.K.; and a Durham University Interdisciplinary Scholarship to G.V. Authors R.L.K. and J.R.K. are affiliated with the Centre for the Coevolution of Biology and Culture at Durham.
Electronic supplementary material
Rights and permissions
About this article
Cite this article
Kendal, R.L., Custance, D.M., Kendal, J.R. et al. Evidence for social learning in wild lemurs (Lemur catta). Learning & Behavior 38, 220–234 (2010). https://doi.org/10.3758/LB.38.3.220
Received:
Accepted:
Issue Date:
DOI: https://doi.org/10.3758/LB.38.3.220